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Factors controlling the dendritic arborization of retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

David Troilo ,
Meijuan Xiong ,
Justin C. Crowley  and
Barbara L. Finlay
David Troilo
Affiliation:
Section of Neurobiology and Behavior and Department of Psychology, Cornell University, Ithaca
Meijuan Xiong
Affiliation:
Section of Neurobiology and Behavior and Department of Psychology, Cornell University, Ithaca
Justin C. Crowley
Affiliation:
Section of Neurobiology and Behavior and Department of Psychology, Cornell University, Ithaca
Barbara L. Finlay
Affiliation:
Section of Neurobiology and Behavior and Department of Psychology, Cornell University, Ithaca
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Abstract

The effects of changing retinal ganglion cell (RGC) density and availability of presynaptic sites on the development of RGC dendritic arbor in the developing chick retina were contrasted. Visual form deprivation was used to induce ocular enlargement and expanded retinal area resulting in a 20–30% decrease in RGC density. In these retinas, RGC dendritic arbors increased in a compensatory manner to maintain the inner nuclear layer to RGC convergence ratio in a way that is consistent with simple stretching; RGC dendritic arbors become larger with increased branch lengths, but without change in the total number of branches. In the second manipulation, partial optic nerve section was used to produce areas of RGC depletion of approximately 60% in the central retina. This reduction in density is comparable to the density of locations in the normal peripheral retina. In RGC-depleted retinas, dendritic arbor areas of RGCs in the central retina grow to match the size of normal peripheral arbors. In contrast to the expanded case, two measures of intrinsic arbor structure are changed in RGC-depleted retinas; the branch density of RGC dendrites is greater, and the relative areas of the two arbors of bistratified cells are altered. We discuss the potential roles of retinal growth, local RGC density, and availability of presynaptic terminals in the developmental control of RGC dendritic arbor.

Keywords

ChicksDendritic arborizationOptic nerve sectionRetinal developmentVisual deprivation
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 4 , July 1996 , pp. 721 - 733
Copyright
Copyright © Cambridge University Press 1996

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References

Adler, R. (1993). Determination of cellular types in the retina. Investigative Ophthalmology and Visual Science 34, 1677–1681.Google ScholarPubMed
Beazley, L.D., Perry, V.H., Baker, B. & Darby, J.E. (1987). An investigation into the role of ganglion cells in the regulation of division and death of other retinal cells. Developmental Brain Research 33, 169–184.CrossRefGoogle Scholar
Bloomfield, S.A. & Hitchcock, P.P. (1991). The dendritic arbors of large-field ganglion cells show scaled growth during expansion of the goldfish retina: A study of morphometric and electrotonic properties. Journal of Neuroscience 11, 910–917.CrossRefGoogle ScholarPubMed
Bodnarenko, S.R. & Chalupa, L.M. (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364, 144–146.CrossRefGoogle Scholar
Cepko, C. (1993). Lineage versus environment in the embryonic retina. Trends in Neuroscience 16, 96–97.CrossRefGoogle ScholarPubMed
Crandall, J.E., Misson, J.P. & Butler, D. (1990). The development of radial glia and radial dendrites during barrel formation in the rat somatosensory cortex. Developmental Brain Research 55, 87–94.CrossRefGoogle Scholar
Crowley, J.C., Xiong, M., Rubin, B.D. & Finlay, B.L. (1995). Developmental control of retinal bipolar cell arborization and stratification following induced retinal enlargement. Society for Neuroscience Abstracts 21, 1770.Google Scholar
Dann, J.F., Buhl, E.H. & Peichl, L. (1988). Postnatal dendritic maturation of alpha and beta cells in cat retina. Journal of Neuroscience 8, 1485–1499.CrossRefGoogle ScholarPubMed
Deich, C., Seifert, B., Peichl, L. & Reichenbach, A. (1994). Development of dendritic trees of rabbit retinal alpha ganglion cells: Relation to differential retinal growth. Visual Neuroscience 11, 979–988.CrossRefGoogle ScholarPubMed
Demello, L.R., Foster, T.M. & Temple, W. (1993). The effect of increased response requirements on discriminative performance of the domestic hen in a visual acuity task. Journal of the Experimental Analysis of Behavior 60, 595–609.CrossRefGoogle Scholar
Deplano, S., Ratto, G.M. & Bisti, S. (1994). Interplay between the dendritic trees of alpha and beta ganglion cells during the development of the cat retina. Journal of Comparative Neurology 342, 152–160.CrossRefGoogle ScholarPubMed
Dreher, B. & Robinson, S.R. (1988). Development of the retinofugal pathway in birds and mammals: Evidence for a common timetable. Brain, Behavior, and Evolution 31, 369–390.Google ScholarPubMed
Ehrlich, D. (1981). Regional specializations of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. Journal of Comparative Neurology 195, 643–657.CrossRefGoogle ScholarPubMed
Eysel, U.T., Peichl, L. & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and critical period. Journal of Comparative Neurology 242, 134–145.CrossRefGoogle Scholar
Finlay, B.L. (1992). Cell death and the creation of regional differences in neuronal numbers. Journal of Neurobiology 23, 1159–1171.CrossRefGoogle ScholarPubMed
Godement, P., Vanselow, J., Thanos, S. & Bonhoeffer, F. (1987). A study in developing visual systems with a new method of staining neurons and their processes in fixed tissue. Development 101, 697–713.CrossRefGoogle ScholarPubMed
Goldstein, L.A., Kurz, E.M., Kalkbrenner, A.E. & Sengelaub, D.R. (1993). Changes in dendritic morphology of rat spinal motoneurons during development and after unilateral target deletion. Developmental Brain Research 73, 151–163.CrossRefGoogle ScholarPubMed
Greenough, W.T. (1986). What's special about development? Thoughts on the bases of experience-sensitive synaptic plasticity. In Developmental Neuropsychobiology, ed. Greenough, W.T. & Juraska, J.M., pp. 387–408. San Diego, California: Academic Press.Google Scholar
Hayes, W.P. & Meyer, R.L. (1988). Optic synapse number but not density is constrained during regeneration onto a surgically halved tecturn in goldfish: HRP-EM evidence that optic fibers compete for fixed numbers of postsynaptic sites on the tectum. Journal of Comparative Neurology 274, 539–559.CrossRefGoogle Scholar
Hitchcock, P.F. (1993). Mature, growing ganglion cells acquire new synapses in the retina of the goldfish. Visual Neuroscience 10, 219–224.CrossRefGoogle ScholarPubMed
Hitchcock, P.F. & Easter, S.S. (1986). Retinal ganglion cells in goldfish: A qualitative classification into four morphological types and a quantitative study of the development of one of them. Journal of Neuroscience 6, 1037–1050.CrossRefGoogle Scholar
Kirby, M.A. & Chalupa, L. (1986). Retinal crowding alters the morphology of retinal ganglion cells. Journal of Comparative Neurology 251, 532–541.CrossRefGoogle Scholar
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
Kossel, A., Lowel, S. & Bolz, J. (1995). Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. Journal of Neuroscience 15, 3913–3926.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Schall, J.D. & Ault, S.J. (1988). Extrinsic determinants of ganglion cell structure in the cat. Journal of Neuroscience 8, 2028–2038.CrossRefGoogle ScholarPubMed
Linden, R. & Perry, V.H. (1982). Ganglion cell death within the developing retina: A regulatory role for retinal dendrites? Neuroscience 7, 2813–2827.CrossRefGoogle ScholarPubMed
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 382–402.CrossRefGoogle ScholarPubMed
Montague, P.R. & Friedlander, M.J. (1989). Expression of an intrinsic growth strategy by mammalian retinal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 86, 7223–7227.CrossRefGoogle ScholarPubMed
Montague, P.R. & Friedlander, M.J. (1991). Morphogenesis and territorial coverage by isolated mammalian retinal ganglion cells. Journal of Neuroscience 11, 1440–1457.CrossRefGoogle ScholarPubMed
Nishimura, Y., Inoue, Y. & Shimai, K. (1979). Morphological development of retinal ganglion cells in the chick embryo. Experimental Neurology 64, 44–60.CrossRefGoogle ScholarPubMed
Norton, T.T. (1990). Experimental myopia in tree shrews. In Myopia and the Control of Eye Growth, Ciba Foundation Symposium 155, ed. Bock, G. & Widdows, K., pp. 178–199. Chichester, England: J. Wiley & Sons.Google Scholar
Pallas, S.L. & Finlay, B.L. (1989). Conservation of receptive-field properties of superior colliculus cells after developmental rearrangements of retinal input. Visual Neuroscience 2, 121–135.CrossRefGoogle ScholarPubMed
Perry, V.H. (1989). Dendritic interactions between cell populations in the developing retina. In Development of the Vertebrate Retina, ed. Finlay, B.L. & Sengelaub, D.R., pp. 149–171. New York: Plenum Press.CrossRefGoogle Scholar
Rager, G. & Rager, U. (1976). Generation and degeneration of retinal ganglion cells in the chick. Experimental Brain Research 25, 551–553.CrossRefGoogle Scholar
Ramoa, A.F., Campbell, G. & Schatz, C.J. (1988). Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. Journal of Neuroscience 8, 4239–4261.CrossRefGoogle ScholarPubMed
Ramon y Cajal, S. (1933). The Structure of the Retina (Thorpe, S.A. & Glickstein, M., Translation). Springfield, Illinois: Charles C. Thomas.Google Scholar
Raviola, E. & Wiesel, T.N. (1985). An animal model of myopia. New England Journal of Medicine 312, 1609–1615.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior, and Evolution 23, 121–164.Google ScholarPubMed
Rohrer, B., Schaeffel, F. & Zrenner, E. (1992). Longitudinal chromatic aberration and emmetropization: Results from the chicken eye. Journal of Physiology 449, 363–376.CrossRefGoogle ScholarPubMed
Rohrer, B., Spira, A.W. & Stell, W.K. (1993). Apomorphine blocks form-deprivation myopia in chickens by a dopamine D2-Receptor mechanism acting in retina or pigmented epithelium. Visual Neuroscience 10, 447–453.CrossRefGoogle ScholarPubMed
Sakaguchi, D.S. (1989). The development of retinal ganglion cells deprived of their targets. Developmental Biology 134, 103–111.CrossRefGoogle ScholarPubMed
Schaeffel, F. & Howland, H.C. (1988). Visual optics in normal and ametropic chickens. Clinical Vision Science 3, 83–98.Google Scholar
Schall, J.D. & Leventhal, A.G. (1987). Relationships between ganglion cell dendritic structure and retinal topography in the cat. Journal of Comparative Neurology 257, 149–159.CrossRefGoogle ScholarPubMed
Snow, R.L., Robson, J.A. & Stelzner, D.J., (1994). Dendritic differentiation of retinal ganglion cells in chick. Society for Neuroscience Abstracts 20, 1492.Google Scholar
Stone, R.A., Lin, T., Laties, A.M. & Iuvone, P.M. (1989). Retinal dopamine and form-deprivation myopia. Proceedings of the National Academy of Sciences of the U.S.A. 86, 704–706.CrossRefGoogle ScholarPubMed
Stryker, M.P. (1991). Activity dependent reorganization of afferents in the developing mammalian visual system. In Development of the Visual System, ed. Lam, D.M.-K. & Shatz, C.J., pp. 267–288. Cambridge, Massachusetts: MIT Press.Google Scholar
Teakle, E.M., Wildsoet, C.F. & Vaney, D.I. (1993). The spatial organization of tyrosine hydroxylase-immunoreactive amacrine cells in the chicken retina and the consequences of myopia. Vision Research 33, 2382–2396CrossRefGoogle ScholarPubMed
Thanos, S., Vanselow, J. & Mey, J. (1992). Ganglion cells in the juvenile chick retina and their ability to regenerate axons in vitro. Experimental Eye Research 54, 377–391.CrossRefGoogle ScholarPubMed
Troilo, D., Gottlieb, M.D. & Wallman, J. (1987). Visual deprivation causes myopia in chicks with optic nerve section. Current Eye Research 6, 993–999.CrossRefGoogle ScholarPubMed
Troilo, D., Howland, H.C. & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 1301–1310.CrossRefGoogle ScholarPubMed
Troilo, D. & Judge, S.J. (1993). Ocular development and visual deprivation myopia in the common marmoset (Callithrix jacchus). Vision Research 33, 1311–1324.CrossRefGoogle ScholarPubMed
Troilo, D., Xiong, M., Crowley, J.C. & Finlay, B.L. (1994 a). Factors controlling dendritic arborization of ganglion cells. Society for Neuroscience Abstracts 20, 1081.Google Scholar
Troilo, D., Xiong, M., Dorries, K., Crowley, J.C. & Finlay, B.L. (1994 b). Changes in retinal ganglion cell density and dendritic arborization following induced retinal enlargement. Investigative Ophthalmology and Visual Science (Suppl.) 35, 2068.Google Scholar
Wallman, J. & Adams, J.I. (1987). Developmental aspects of experimental myopia in chicks. Vision Research 27, 1139–1163.CrossRefGoogle ScholarPubMed
Wallman, J., LeDoux, C. & Friedman, M.B. (1978). Simple devices for restricting the visual fields of birds. Behavioral Research Methods and Instrumentation 10, 401–403.CrossRefGoogle Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1981 a). Morphology and topography of on and off-alpha cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157–175.Google Scholar
Wässle, H., Peichl, L. & Illing, R.-B. (1981 a). Morphology and topography of on- and off-beta cells in the cat retina. Proceedings of the Royal Society B (London) 212, 177–195.Google Scholar
Wingate, R.J.T. & Thompson, I.D. (1994). Targeting and activity-related dendritic modification in mammalian retinal ganglion cells. Journal of Neuroscience 14, 6621–6637.CrossRefGoogle ScholarPubMed
Wong, R.O.L. (1990). Differential growth and remodelling of ganglion cell dendrites in the postnatal rabbit retina. Journal of Comparative Neurology 294, 109–132.CrossRefGoogle ScholarPubMed
Wong, R.O.L., Hermann, K. & Shatz, C.J. (1991). Remodeling of retinal ganglion cell dendrites in the absence of action potential activity. Journal of Neurobiology 22, 685–697.CrossRefGoogle ScholarPubMed
Xiong, M., Crowley, J.C., Troilo, D., Kelly, M. & Finlay, B.L. (1995). Developmental control of dopaminergic amacrine cell arborization following partial optic nerve section. Society for Neuroscience Abstracts 21, 1770.Google Scholar
Xiong, M.J. & Finlay, B.L. (1993). Changes in synaptic density after developmental compression or expansion of retinal input to the superior colliculus. Journal of Comparative Neurology 330, 455–463.CrossRefGoogle ScholarPubMed
Xiong, M., Pallas, S.L., Lim, S. & Finlay, B.L. (1994). Regulation of retinal ganglion cell axon arbor size by target availability: Mechanisms of compression and expansion of the retinotectal projection. Journal of Comparative Neurology 344, 581–597.CrossRefGoogle ScholarPubMed